Feeding behaviour and functional morphology of the feeding ...

Marine Biology Research, 2006; 2: 77 88

ORIGINAL ARTICLE

Feeding behaviour and functional morphology of the feeding appendages of red king crab Paralithodes camtschaticus larvae

A. EPELBAUM & R. BORISOV Crustacean Reproduction Laboratory, Russian Federal Research Institute of Fisheries and Oceanography (VNIRO), 17 V. Kranoselskaya St., 107140 Moscow, Russia

Abstract The aim of the study was to examine the feeding mechanism of planktonic larvae (pre-zoea, zoeae I IV) of the red king crab using a combination of morphological and behavioural data obtained under laboratory conditions. Feeding appendages and accompanying setal types of larvae are described, illustrated, and related to their functions during prey capture and ingestion. Descriptions are based on direct behavioural observations of larvae fed several types of food and on theoretical assumptions based on the morphology of the appendages and body parts involved in feeding. The pre-zoea is covered by embryonic cuticle and does not feed. Under laboratory conditions, zoeae I IV show a mixed feeding strategy: they are able to feed by the capture of material suspended in the water column and by the collection of food objects from the substratum. Zoeae are able to capture and ingest a relatively wide range of particle sizes, from 100 mm to 2 mm, and are highly cannibalistic; they do not show true hunting behaviour and rely on an ‘‘encounter feeding’’ mechanism. An analysis of larval feeding behaviour is presented and its implications for larval cultivation are considered. Recommendations on possible sizes, concentrations and distribution of food objects in the rearing tanks are outlined.

Key words: Cannibalism, feeding behaviour, functional morphology, red king crab, zoea

Introduction Most studies of the functional morphology of the mouthparts of decapod crustacean larvae have merely focused on descriptions of morphological features. Only a few studies have integrated data on morphology and behaviour (e.g. Gonor & Gonor 1973); a comprehensive analysis of the functions of the mouthparts of decapod zoeae based on videographed records of feeding activity has recently been made by Crain (1999) for Placetron wosnessenskii . Behavioural observations in conjunction with detailed morphological descriptions are very important for relating form and function of the mouthparts of crustaceans. These studies also aid in understanding the feeding requirements and preferences of different life phases of a given species, thus helping to establish rearing methods for both research and commercial cultivation. Our study focused on the feeding behaviour of the larvae of the red king crab, Paralithodes camtschaticus

(Tilesius, 1815) (Decapoda, Anomura, Lithodidae), one of the most commercially important species of crustaceans. The red king crab has a broad distributional range in the North Pacific Ocean and now also in the North Atlantic, to where it was transplanted in the 1960s. It has a reproductive cycle with mating in spring, brooding for almost a year, and hatching from March to April (Shirley & Shirley 1989; Bakanev & Kuzmin 1999). The larvae hatch out as pre-zoeae, pass through four zoeal stages and moult to the glaucothoe stage, during which settlement occurs. Recent studies suggest that lithodid crabs from high latitudes show a tendency towards lecithotrophy, i.e. a food-independent, endotrophic mode of larval development (Thatje et al. 2005 and earlier studies cited therein), which is mainly based on a degradation of internal lipid reserves remaining from the egg yolk (Kattner et al. 2003). Complete larval independence of external food sources has been interpreted as a reproductive adaptation to conditions typically

Correspondence: A. Epelbaum, Crustacean Reproduction Laboratory, Russian Federal Research Institute of Fisheries and Oceanography (VNIRO), 17 V. Kranoselskaya St., 107140 Moscow, Russia. E-mail: anna_epelbaum@hotmail.com, epelbaum@vniro.ru Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark (Accepted 4 March 2006; Printed 6 June 2006) ISSN 1745-1000 print/ISSN 1745-1019 online # 2006 Taylor & Francis DOI: 10.1080/17451000600672529

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prevailing at high latitudes, i.e. cold stress and seasonally short or unpredictable plankton productivity in winter and spring (Anger et al. 2003). All lithodid species from the southern hemisphere studied so far show a lecithotrophic mode of larval development, which is explained by their presumable origin from deep-sea ancestors (Thatje et al. 2005). Food-independent larval development has also been observed in two lithodids from the northern hemisphere (Anger 1996; Shirley & Zhou 1997). However, red king crab zoeae are known to be planktotrophic (e.g. Kurata 1960; Paul & Paul 1980). Although several studies have been made on the morphology and feeding of red king crab larvae (e.g. Marukawa 1933; Sato & Tanaka 1949; Kurata 1960; Paul & Paul 1980; Nakanishi 1987; Abrunhosa & Kittaka 1997; Kittaka et al. 2002; Epelbaum & Kovatcheva 2005), knowledge of their functional morphology and feeding behaviour is still scarce. The aim of our study was to obtain a comprehensive understanding of the functional morphology and feeding mechanisms of P. camtschaticus larvae using a combination of morphological studies and behavioural observations under laboratory conditions. Material and methods The study was conducted at the Laboratory of Crustacean Reproduction of the Russian Federal Research Institute of Fisheries and Oceanography (VNIRO, Moscow) and the Biological Faculty of the Moscow State University in 2001 2004. Larval culture Ovigerous females of the red king crab were caught using baited traps at the end of February each year in Ura Bay, Barents Sea, and transported to Moscow in 60 l isothermal boxes supplied with an aeration system at 1.5 38C. After thermal acclimation, females were placed into 1 m3 holding tanks with a recycling water system; the water temperature was maintained at 5.09/0.58C and salinity at 32 33 ppm. Artificial seawater was prepared using marine salt HW-Marinemix professional (Wiegandt, Krefeld, Germany). Females were fed fresh frozen mussel, squid, and shrimp meat. The hatching of larvae usually occurred in March and lasted for approximately 3 days. After mass hatching, larvae were scooped up using a 1.5 mm mesh net and transferred into six 160 l rearing tanks with recycling water. The initial rearing density in each tank was 50 larvae l 1 (Kovatcheva 2001). The water temperature was maintained at 7.0 8.08C and salinity at 3233 ppm. The larvae were fed freshly hatched

nauplii of Artemia sp. two to three times a day in accordance with the maximum daily ration at each developmental stage (for details see Epelbaum & Kovatcheva 2005). Morphological studies Measurements and morphological descriptions were made following basic procedures and using the terminology of Sato & Tanaka (1949), Konishi & Quintana (1987) and Abrunhosa & Kittaka (1997). For morphological studies, larvae and exuvia were fixed and preserved in 4% formalin. The arrangement, morphology and setation of the appendages were examined from individuals and their exuvia under dissecting and compound microscopes with ocular grids. Ink line drawings were made on grid paper. Because most oral appendages are flattened and layered, the terms ‘‘inner surface’’ (towards the mouth) and ‘‘outer surface’’ (away from the mouth) were used for descriptions; for example, the outer surface of the maxillule is adjacent to the inner surface of the maxilla. The drawings illustrate left appendages from the outer side unless otherwise indicated. The setal types are described following the general terminology of Factor (1978), based largely on the nature and distribution of the setules. We modified Factor’s descriptions slightly for red king crab larvae, having differentiated eight setal categories: Plumose setae (Pls, Factor’s type A) bear two distinct rows of densely arranged long setules along most of the shaft length, and may be segmented by annulations. Pappose setae (Pps, Factor’s types B1 and B2) have long setules similar to those of plumose setae, but loosely arranged about the shaft in a random manner. Plumodenticulate setae (Pds, Factor’s types C1 C4) bear long sparse setules in the proximal half and two rows of tooth-like setules in the distal half of the shaft. The two regions may be separated by a bulbous swelling of the shaft. Serrulate setae (Srls, Factor’s type F1) bear short peg-like setae (denticulations) arranged in two rows along most of the length of the shaft. The distal portion can appear as a stiletto with very small denticulations. Cuspidate setae (Cs, Factor’s types H1 and H2) are large and conical-shaped and may have one row of fine, tooth-like setules. Simple setae (Ss, Factor’s type I) are relatively thin and lack setules or any other secondary processes. Plumed-pappose setae (Plps, not differentiated by Factor) bear long setules along most of the length of the shaft growing mostly in two directions.

Feeding of red king crab larvae Hair-like structures (Hs, not differentiated by Factor) resemble the setules of plumose setae in form and size. The setules are in most cases drawn schematically or omitted, in order to avoid the obfuscation of illustrated appendages.

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Additionally, we conducted an experiment aimed at evaluating the maximum survival time of starved larvae. Eight newly hatched pre-zoeae were placed individually into 60 ml glass vials and were not fed. In this experiment, the confounding effect of cannibalism was avoided. Results

Behavioural observations and short-term feeding experiments Zoeae were observed while they were swimming freely in 160 l tanks and 0.8 1.0 l glass containers, to which they were transferred by means of a largebore pipette. Additional observations of zoeae swimming in small glass vessels containing 20 ml of seawater were made by means of a dissecting microscope. Swimming zoeae were also videotaped using a Panasonic NV-GS400 video camera with a Raynox 2.5 /macro lens. The analysis of behavioural patterns was based on a review of the videotapes at both normal speed (25 frames s 1) and in slow motion (stepping through individual frames). In order to study the feeding behaviour of the larvae, several types of potential foods having different characteristics (vitality, size, buoyancy) were added to the experimental glass containers and vessels. The following food types were used: brine shrimp (Artemia sp.) nauplii and two types of artificial agglomerated feed for larval marine fish and crustaceans: Start 100 and Start 300 (Dana Feed A/ S, Denmark), with particle sizes of 90 200 and 150 400 mm, respectively. The nauplii were added at an initial concentration of 800 1000 nauplii l 1; artificial feeds were added at a concentration of 4050 mg l 1. The aim of these feeding experiments was to observe the behaviour of the larvae while they were offered different food objects, in particular swimming and the capture of food. Daily food intakes, the development, survival and growth performance of red king crab larvae in relation to these dietary treatments were not the scope of this study, but are described and discussed in separate papers (Kovatcheva & Epelbaum 2003; Epelbaum & Kovatcheva 2005; Epelbaum et al. 2005). To evaluate the cannibalistic behaviour of the larvae, we placed active newly hatched pre-zoeae into two containers with 0.8 l of gently aerated seawater at 7 88C at a density of 50 individuals l 1, i.e. 40 larvae per container. The larvae in the first container were fed Artemia nauplii, whereas those in the second container were not fed. Thirty minute observations on larval behaviour were conducted every day at 12.00 for 5 days. The experiment was continued until all starved larvae died.

Morphology and behaviour of the pre-zoea Morphological characteristics. The body of the prezoea is covered with a thin envelope an embryonic cuticle. The cuticle forms soft plumose processes with thin walls on the antennules, antennae and telson (Figure 1A, E). The appendages of the prezoea have the same morphological characteristics as those of the first stage zoea, but are covered by embryonic cuticle, and most setae are still unextruded (Figure 1A D). Behavioural patterns. Pre-zoeae swim up to the surface from time to time and then slowly sink back to the bottom. They do not have swimming setae on the exopodites of maxillipeds and swim in zigzag movements by flexing and extending their abdomens. The telson, with its cuticular processes, acts as a primary blade (or paddle). When the pre-zoea stops abdominal movements, cuticular processes on antennules and antennas open like a fan and slacken the rate of sinking. Pre-zoeae are positively phototactic. Experiments run at 7 88C revealed that the prezoeal phase normally lasts for less than 1 h. Moulting occurs quickly, with the larva emerging from the prezoeal cuticle and the setae on its appendages turning out in several minutes. Pre-zoeae that did not moult within 1.5 h from hatching showed various morphological abnormalities: underdeveloped setae on the appendages, a deformed rostrum, etc. These larvae were largely inactive and died within 10 days, showing various degrees of abnormal development (Figure 2).

Morphology and behaviour of zoeae IIV Arrangement and morphology of body parts and appendages involved in feeding (Figure 3A). The gross morphology of the body parts and appendages remain essentially the same throughout the whole zoeal phase. With each moult, larval appendages become proportionally larger. Some appendages, mainly those involved in creating water currents (i.e. maxillae and maxillipeds), acquire additional setae and/or segments and parts. Detailed morphological descriptions of all larval and early juvenile

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Figure 1. Morphological features of the pre-zoea. (A) Antenna, (B) maxillula, (C) maxilla, (D) second maxilliped, (E) telsonal seta covered by plumose cuticular process. Scale bars: 0.2 mm.

stages of the red king crab are given in Epelbaum et al. (2006). Thus, in the present paper we are only briefly concerned with the main morphological features of the larval appendages involved in the capture and/or manipulation and ingestion of food. The pre-oral chamber is formed by the labrum, a relatively large lobe with a dense group of simple setae along the lower margin (Figure 3B), and by the lobes of the paragnaths covered by numerous simple setae. The sides of the chamber are bordered by plate-like and asymmetrical mandibles (Figure 3C); the cutting edges of the mandibles are aligned in a ventro-dorsal plane, perpendicular to the sagittal plane of the larva; the bud of the mandibular palp is present only in zoea IV. Each flattened maxillule

(Figure 3D) has a setose coxal endite, a toothed basal endite and an endopodite. The maxillae (Figure 3E) consist of coxal and basal endites bearing plumodenticulate setae, an unsegmented endopodite and a large exopodite (scaphognathite) with 5/9/11/13 widely spaced plumed-pappose setae along the distal margin in zoeae IIV, respectively. The margins of the scaphognathite and the endopodite, along with the margins and internal surfaces of the endites, bear thin hair-like structures, in form and size resembling the setules of plumose setae. These structures remain on the maxillae throughout the whole zoeal phase. Each of the three pairs of maxillipeds consists of a massive protopodite, endopodite and exopodite. The first and second maxillipeds are morphologically alike and

Figure 2. Morphological abnormalities in the larvae: (A) maxillula, (B) maxilla. Scale bar: 0.2 mm.

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Figure 3. Fourth stage zoea. (A) Diagram of the ventral view showing the arrangement of the appendages, (B) labrum, (C) mandible, (D) maxillule, (E) maxilla, (F) maxilliped I. Scale bars: (A) 1 mm, (B) (F) 0.2 mm. Abbreviations: lbr, labrum; mnd, mandible; mx I, maxillule; mx II, maxilla; mxp I III, maxillipeds I III; pgn, paragnaths. For setal type abbreviations, see Material and methods section.

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remain generally the same throughout the zoeal phase: they only acquire additional plumose setae on the outer margins of the endopodites and plumose natatory setae on the distal segments of the exopodites; each natatory seta has two annulations allowing it to bend. In zoea I, the outer margins of the endopodites of the first and second maxillipeds are covered with thin hair-like structures, probably the same as those found on the maxillae. The third maxilliped is underdeveloped in zoea I: the protopodite bears unsegmented non-setose elongated buds of the endo- and exopodite. In zoeae IIIV, the exopodite is bi-segmented and bears 6/8/8 plumose natatory setae, respectively, with three annulations each. The posterior margin of the telson is cleft medially to form lateral lobes, with seven stout serrulate setae each. Behavioural patterns. Zoeae swim primarily by beating movements of the maxillipedal exopodites, which bear long natatory setae. These setae form somewhat concave blades (Figure 3A). Rapid beating of the exopodites downward and anteriorly (Figure 4) creates a current directed towards the rostrum; this current sends the larva backwards with its posterior carapace spines and telson leading. Therefore, by beating the exopodites, the larva predominantly

swims vertically upwards. The analysis of videotaped swimming activity of larvae demonstrated that at 7 88C they typically perform from eight to 13 maxillipedal strokes per second. The beating movements of the maxillipeds are successive, i.e. nonsynchronous (Figure 4A). With the exopodites motionless, the larva descends in the water column. It is also able to actively swim downwards, with its abdomen flexed, the protopodites of the maxillipeds held proximate to the abdomen, and dorsal carapace spines pointed downwards. However, this swimming mode was only observed as a quick short-time response to light stimulus coming from the bottom of the observational container. The larva adjusts the direction of swimming by changing the position of its maxillipeds and telson. The maxillipedal endopodites are always held extended anteriorly (Figure 4) and were never observed to function in swimming. Zoeae were observed to consume all types of food tested during the experiments. When food items were added to the experimental containers, zoeal locomotory behaviour did not change significantly: no hunting behaviour such as that reported for zoeae of some other decapod species (e.g. Knudsen 1960) was observed. When a potential food object suspended in the water column approached the thoracic

Figure 4. Movements of the maxillipeds of the zoea. (A) The position during the stroke, (B) the position after the stroke.

Feeding of red king crab larvae region of the larva close to maxillipedal exopodites, the larva immediately captured this object using maxillipedal endopodites and sometimes dragged its telson posteriorly across the mouthparts. Zoeae also collected food from the bottom they were observed to feed on weak nauplii of Artemia sp. and on the particles of artificial feeds Start 100 and Start 300 (these feeds sunk to the bottom in approximately 1 h after being added to experimental containers). The larva either approached a potential food object by passively sinking with maxillipedal exopodites motionless or swam to it from the side. When the larva approached the food object with its telsonal or maxilipedal area first, the act of capture as described above typically occurred. However, when the food object touched the zoea’s rostrum or any portion of the carapace first, the larva moved away, apparently showing avoidance behaviour. The behavioural patterns described above remained generally the same throughout the whole zoeal phase. Of the various food objects offered, freshly hatched Artemia sp. nauplii were consumed most willingly and provided the highest survival rates of the larvae (Epelbaum et al. 2005). All four zoeal stages were observed to be highly cannibalistic, especially when they received no food (Figure 5): when nauplii of Artemia sp. were used as food, 16.4% of the larvae were killed and partly consumed by their conspecifics, whereas among the

Figure 5. Cannibalistic behaviour of the first stage zoea.

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unfed group-reared larvae the level of cannibalism reached 25%. Dead individuals that had already become colourless were also observed being consumed. Sixty per cent of unfed larvae died by day 10, still in the first zoeal stage at the same time that the larvae fed Artemia nauplii successfully moulted to the second stage. Only one unfed larva managed to moult to the second zoeal stage on day 11, but died 2 days later. The last larva died on day 17. In the experiment where the larvae were reared individually and received no food, none of the larvae managed to moult to the second zoeal stage. By day 10, 25% of starved individually reared larvae died. The average survival time of starved larvae was 159/3.6 days. The last larva died on day 20: its survival time was twice the normal duration of the first zoeal stage in fed larvae (see Epelbaum & Kovatcheva 2005). Discussion Behavioural and morphological analysis of larval feeding mechanisms Pre-zoea. The main morphological feature found in the pre-zoea, an embryonic cuticle covering the pre-zoea’s body, has been described for the prezoea of many other decapod species (e.g. Gonor & Gonor 1973; Konishi 1987; Hong 1988; Guerao & Abello 1996). This cuticle, which forms long plumose projections in the antennal and telsonal areas, is well modified for swimming. We assume that it is impractical for the larva to have rigid fully developed setae when it is rolled up inside the egg, so it hatches out with its setae still folded. The presence of embryonic cuticle projections allows it to move relatively quickly, and the larvae can thus disperse immediately after hatching. Another argument was offered by Gonor & Gonor (1973) in support of the interpretation of the pre-zoeae of porcellanid crabs as a natural stage, not a laboratory artefact: a short-lived, rounded larva with few body projections would more effectively escape entangling detrital material on the bottom immediately after hatching. As long as the setae of the short-lived pre-zoea are confined beneath the cuticle, there is no feeding during this stage. In our experiments, pre-zoeae that survived but did not moult within 1.5 h of hatching showed alterations in the normal pattern of appendage setation. The consequences of such abnormalities were: (1) abnormal zoeal locomotion, which in turn caused a reduction in the mobility of the larvae, and, more importantly, (2) that the normal feeding process, which normally starts on the first day of hatching, was impossible. Abnormal setation of the

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appendages was described in larvae of several species of brachyuran crabs when previous larval instars were exposed to high concentrations of toxic substances (Rodrı´guez & Pisano´ 1993; Rodrı´guez & Medesani 1994; Lo´pez Greco et al. 2001). These toxicologically induced abnormalities could be the result of inhibition/modification of the hormones involved in the processes of morphogenesis and moulting (Lo´pez Greco et al. 2001). In the present case, the abnormalities may have occurred due to the fact that some pre-zoeae did not have enough energy reserve for the moulting process, and the setae of the first zoeal instars started to develop inside the old exuvia. These abnormalities may also have been a consequence of somewhat ‘‘premature’’ hatching: certain laboratory conditions could have facilitated larval release, and thus some pre-zoeae were still underdeveloped by the time of hatching. This assumption is supported by the fact that other species of lithodids are reported to have extended periods of larval hatching, of the order of several weeks (e.g. Paul & Paul 2001; Thatje et al. 2003), which may be a typical reproductive pattern for lithodids. Study of the hatching of the red king crab under various environmental conditions may reveal the reasons underlying larval developmental abnormalities and may also aid in understanding the physiological plasticity of this species. Zoea. After the pre-zoea sheds the embryonic cuticle and transforms to the zoea I, its behaviour changes. By actively beating the maxillipedal exopodites, the zoea swims backwards with its telson leading, like

the larvae of many other decapod crustaceans (Foxon 1936). The current generated by the exopodites creates a circulation of water near the sides and ventral surface of the larva. The oral part of this circulation may be considered as a feeding current, directed anteriorly towards the labrum, parallel to the longitudinal axis of the body (Figure 6A). When the zoea swims actively, small food objects that pass near its thoracic or abdominal region are caught by the feeding current and delivered to the maxillipedal endopodite area. When the larva descends in the water column with its maxillipedal exopodites motionless, it may passively approach food items (Figure 6B). Therefore, we distinguish between ‘‘active’’ and ‘‘passive’’ modes of prey capture. The ‘‘active’’ mode is probably more effective when capturing small food objects (e.g. nauplii of Artemia sp.), which cannot withstand the feeding current, i.e. those that are caught by the water flow, whereas for capturing large food items comparable to the size of the larvae itself, and objects from the bottom, the ‘‘passive’’ mode may be more advantageous. Therefore, according to our laboratory observations, red king crab larvae show a mixed feeding strategy: they are able to feed by capturing material suspended in the water column and by collecting food objects from the substratum. In both cases, the food item is captured by the maxillipedal endopodites. The telson is probably used to help the endopodites scoop up the food, quickly pushing it towards the oral appendages. On the basis of the endopodite’s morphology, we

Figure 6. Two modes of prey capture: (A) active, (B) passive (solid arrows show the feeding current, the dashed arrows indicate the direction of movement of the zoea).

Feeding of red king crab larvae suppose that the serrulate setae, directed towards the sagittal plane, are used for capturing and holding the food, whereas the pappose setae, directed towards the mouth, serve to pass the food to the maxillae and maxillules. A similar role for the maxillipeds in capturing prey was described for larval crabs of the family Porcellanidae (Gonor & Gonor 1973). However, our observations and assumptions on the role of the maxillipeds and telson in the feeding process contrast with the data of Crain (1999) for the zoeae of the lithodid crab Placetron wosnessenskii , in which the maxillipeds and telson did not take part in prey manipulation and ingestion, and the maxillipeds were used only for locomotion. Plumodenticulate setae on the endites of the maxillae and on the coxal endites of the maxillules probably serve for holding the prey and passing it to the mandibles. Cuspidate setae of the maxillules, lying parallel to the incisor processes of the mandibles, probably tear large food particles, working synergetically with the mandibles. The paragnaths probably prevent the loss of food from the mouth area during mandibular activity, and the labrum assists in the process of food swallowing, along with the oesophageal peristalsis; these functions of the paragnatha and the labrum, which could hardly be directly observed in small larvae, were described for the European lobster Homarus gammarus (Robertson & Laverack 1979). One peculiar feature of the maxillae in all zoeal stages is the presence of thin hair-like structures, which can be observed along the margins of the scaphognathites and endopodites, and on the margins and dorsal surfaces of the endites. Clusters of such hair-like structures were described for the maxillae of the first stage zoeae of Petrolisthes robsonae and were termed ‘‘microtrichia’’ (GarcıáGuerrero et al. 2005). As long as the marginal hairlike structures are filling up the spaces between the component parts of the maxilla, their function may be associated with the water currents created by the maxillae. Hair-like structures on the dorsal surfaces of the endites are located in the space between the maxillae and the maxillules, and therefore may aid in preventing the loss of food particles; these assumptions are indirectly supported by the fact that the non-feeding glaucothoe lacks these structures on the maxillae, whereas feeding juveniles acquire rows of plumose setae in these areas of the maxillae again (Epelbaum et al. 2006). Feeding behaviour of zoeae I IV: implications for culture In recent years there has been a sharp decline in red king crab stocks in many areas of the North Pacific Ocean. The development of feasible techniques for the artificial reproduction and subse-

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quent culture of larvae, followed by release of the juveniles to natural environments, is considered as one of the possible ways of restoring red king crab stocks (Kovatcheva 2001). Laboratory cultivation is also useful for improving knowledge of the early development of this species, which in turn contributes towards establishing strategies for the management of this resource. For successful culture of the red king crab it is important to obtain a comprehensive understanding of various aspects of larval feeding, as food availability and quality are the main limiting factors to larval survival (Paul & Paul 1980; Paul et al. 1989). Under laboratory conditions, the nauplii of Artemia sp. are commonly used as food for red king crab larvae (Kurata 1960; Nakanishi 1987; Epelbaum & Kovatcheva 2005): they represent nutritious, convenient, and easy to produce live food. However, other foods have also been tested for the larvae: several species of diatoms, annelid trochophores, copepods, barnacle nauplii (Sato & Tanaka 1949; Kurata 1959; Paul et al. 1989), and, recently, agglomerated artificial feeds (Epelbaum et al. 2005). Red king crab larvae consumed these feeds, but in all cases larval survival rates were lower compared with those obtained when the larvae were fed brine shrimp nauplii. The testing of new food types that are able to fulfil the nutritional requirements of larvae, as well as the improvement of existing feeding techniques, is an interesting subject for future studies. McConaugha (1985) identified three criteria for determining the suitability of prey items as food for larval crustaceans: (1) appropriate size for capture and consumption, (2) adequate concentration, and (3) nutritional value essential to meet the larva’s needs. Below we discuss the first two criteria in relation to red king crab zoeae. Our experiments indicate that red king crab zoeae are able to capture and ingest a relatively wide range of particle sizes. The maximum size of a zoea’s food objects is probably comparable with the size of the zoea itself and is of the order of 2 mm, taking into account the frequently observed acts of cannibalism. The minimum size is probably limited by the distance between the setae on the maxillipedal endopodites and is estimated to be approximately 100 150 mm. This assumption was supported by the results of the experiments aimed at evaluating the consumption of artificial feeds on the growth and survival of red king crab larvae under laboratory conditions: the larvae were able to capture and consume both the Start 100 and Start 300 feeds, with particle sizes of 90 200 and 150 400 mm, respectively (for details see Epelbaum et al. 2005).

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Our observations indicate that, in spite of the fact that zoeae are good swimmers and have well-developed eyes, they do not use sight in locating and capturing prey. Like the larvae of some porcellanid crabs (Gonor & Gonor 1973), red king crab zoeae do not show true hunting behaviour and appear to rely entirely on chance encounters with prey items. Berkes (1975) termed this feeding mechanism ‘‘encounter feeding’’. The act of food capture may be initiated by direct contact with the setae on the maxillipedal endopodites and/or with the abdomen. Therefore, the survival of zoeae is highly dependent upon an appropriate prey density. Red king crab larvae can effectively capture food objects dispersed in the water only up to a certain concentration. Our past experiments revealed that for zoeae IIV reared at 788C, the Artemia nauplii concentration had to be higher than 160 nauplii l 1 before all zoeae were consistently able to capture and consume at least one nauplius per day. The maximum daily food intakes of zoeae I IV comprised 11.3, 22.4, 33.2 and 41.8 nauplii individual 1 day1, respectively; the initial Artemia nauplii concentrations sufficient for eliciting these maximum daily food intakes were 400 600, 600 800, 800 1000 and 1000 1200 nauplii l 1 for zoeae I IV, respectively (for details see Epelbaum & Kovatcheva 2005). Considering the feeding mechanism described above, when red king crab larvae are cultured under laboratory conditions, it is desirable to provide an even distribution of food in the rearing tanks. Thus, when live organisms having a positive photoresponse, such as brine shrimp nauplii, are used as food, it is recommended to illuminate rearing tanks as evenly as possible: this will favour an even distribution of food objects. When the larvae are fed artificial feeds, it will be advantageous to keep the water constantly aerated by a gentle flow of air from the bottom of the rearing tanks. However, the air flow should be adjusted so that it does not interfere with the swimming of the larvae. Ensuring that food objects are evenly dispersed increases the probability that the zoeae will be able to capture and consume them, thus increasing the probability of the successful development of the larvae. Feeding behaviour of zoeae IIV: ecological implications As described above, under laboratory conditions red king crab larvae were observed to feed by capturing suspended material and by collecting particles from the substratum. However, in the field, the larvae are probably predominantly using the first mode of feeding capturing suspended food objects. The larvae are found in both the upper and lower layers

of the water column and it is suggested that they undergo diurnal vertical migrations (Takeuchi 1962). Therefore, they spend most of the time actively swimming (or adjusting their position) in the water column. In Auke Bay, Alaska, larvae are found in the upper 10 15 m of water during the daytime and in deeper waters at night (Shirley & Shirley 1988). In contrast, in the Bering Sea, zoeae are reported to rise to the surface at night and sink during the day (Takeuchi 1962). Either migratory pattern would allow the larvae to test the water column for prey availability. Under natural conditions, red king crab zoeae are unlikely to encounter zooplankton prey in the concentrations sufficient for eliciting maximum daily food intakes. However, unlike some other lithodids occurring at high latitudes, red king crabs have not developed larval lecithotrophy as an adaptation to nutritionally harsh conditions of polar seas. The ability of red king crab larvae to capture and ingest food objects of various sizes and shapes may probably be considered as an early life-history adaptation to unpredictable plankton productivity: it expands the diversity of prey species that meet McConaugha’s first criterion, and therefore increases the probability that the larvae will be able to fulfil their nutritional requirements and develop successfully. Acknowledgements We are very grateful to Drs N. P. Kovatcheva, V. Y. Pavlov (VNIRO, Russia), N. N. Marfenin (Invertebrate Zoology Department, Moscow State University, Russia) and S. Thatje (National Oceanography Centre, University of Southampton, UK) for their invaluable advice and suggestions. We would also like to thank the research staff at Crustacean Reproduction Laboratory of VNIRO for assistance in the course of the experiments. References Abrunhosa FA, Kittaka J. 1997. Functional morphology of mouthparts and foregut of the last zoea, glaucothoe and first juvenile of the king crabs Paralithodes camtschaticus, P. brevipes and P. platypus . Fisheries Science (Tokyo) 63:923 30. Anger K. 1996. Physiological and biochemical changes during lecithotrophic larval development and early juvenile growth in the northern stone crab, Lithodes maja (Decapoda: Anomura). Marine Biology 126:283 96. Anger K, Thatje S, Lovrich G, Calcagno J. 2003. Larval and early juvenile development of Paralomis granulosa reared at different temperatures: tolerance of cold and food limitations in a lithodid crab from high latitudes. Marine Ecology Progress Series 253:243 51. Bakanev SV, Kuzmin SA. 1999. First results of the investigation on red king crab (Paralithodes camtschaticus ) larvae distribution

Feeding of red king crab larvae in the Barents Sea. In: Proceedings of the International Conference Fishery Research of the World Ocean, Vladivostok, 27 29 September 1999. Vladivostok: Dalribvtuz. p 99 101 (in Russian). Berkes F. 1975. Some aspects of feeding mechanisms of euphausiid crustaceans. Crustaceana 29:266 70. Crain JA. 1999. Functional morphology of prey ingestion by Placetron wosnessenskii Schalfeev zoeae (Crustacea: Anomura: Lithodidae). Biological Bulletin 197:207 18. Epelbaum AB, Borisov RR, Kovatcheva NP. 2006. Early development of the red king crab Paralithodes camtschaticus from the Barents Sea reared in the laboratory. Journal of the Marine Biological Association of the UK 86:317 333. Epelbaum AB, Kovatcheva NP. 2005. Daily food intakes and optimal food concentrations for red king crab (Paralithodes camtschaticus ) larvae fed Artemia nauplii under laboratory conditions. Aquaculture Nutrition 11:455 61. Epelbaum A, Kovatcheva N, Kryakhova N. 2005. The use of artificial feeds for red king crab larvae cultivation. In: Kotenev BN et al., editors. Marine Coastal Ecosystems: Seaweeds, Invertebrates and Products of their Processing. Moscow: VNIRO Publishing. p 175 8 (in Russian). Factor JR. 1978. Morphology of the mouthparts of larval lobsters Homarus americanus (Decapoda: Nephropidae) with special emphasis on their setae. Biological Bulletin 154:383 408. Foxon GEH. 1936. Observations on the locomotion of some arthropods and annelids. Annals and Magazine of Natural History 10:403 19. Garcıá-Guerrero MU, Cuesta JA, Hendrickx ME, Rodrı´guez A. 2005. Larval development of the eastern Pacific anomuran crab Petrolisthes robsonae (Crustacea: Decapoda: Anomura: Porcellanidae) described from laboratory material. Journal of the Marine Biological Association of the UK 85:339 49. Gonor SL, Gonor JJ. 1973. Feeding, cleaning and swimming behaviour in larval stages of porcellanid crabs (Crustacea: Anomura). Fishery Bulletin 71:225 34. Guerao G, Abello P. 1996. Morphology of the prezoea and first zoea of the deep-sea spider crab Anamathia rissoana (Brachyura, Majidae, Pisinae). Scientia Marina (Barcelona) 60:245 51. Hong SY. 1988. The prezoeal in various decapod crustaceans. Journal of Natural History 22:1041 75. Kattner G, Graeve M, Calcagno JA, Lovrich GA, Thatje S, Anger K. 2003. Lipid, fatty acid and protein utilization during lecithotrophic larval development of Lithodes santolla (Molina) and Paralomis granulosa (Jacquinot). Journal of Experimental Marine Biology and Ecology 292:61 74. Kittaka J, Stevens BG, Teshima S, Ishikawa M. 2002. Larval culture of the king crabs Paralithodes camtschaticus and P. brevipes . In: Paul AJ, et al., editors. Crabs in Cold Water Regions: Biology, Management, and Economics. Fairbanks: University of Alaska Sea Grant. p 189 212. Knudsen JW. 1960. Reproduction, life history and larval ecology of the California Xanthidae, the pebble crabs. Pacific Science 14:3 17. Konishi K. 1987. Larval development of spiny sand crab Lophomastix japonica (Durufle, 1889) (Crustacea, Anomura, Albuneidae) under laboratory conditions. Publications of the Seto Marine Biological Laboratory 32:123 39. Konishi K, Quintana R. 1987. The larval stages of Pagurus brachiomastus (Thallwitz, 1892) (Crustacea, Anomura) reared in the laboratory. Zoological Science 4:349 65. Kovatcheva NP. 2001. Method of crustacean reproduction (red king crab). Russian Federation Patent No. 2200386. Declared 27 December 2001. Published 20 March 2003. Bull. 8 (in Russian).

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